Relationship between fiber capillarization and mitochondrial volume density in control and trained rat soleus and plantaris muscles.

Abstract

The majority of investigations have demonstrated a strong relationship between muscle capillarity and oxidative capacity. There is, however, evidence that the capacities for O2 supply and utilization can be dissociated. Also, metabolite removal rather than O2 supply may represent the predominant design constraint placed on the capillary bed in some muscles (i.e, fast-twitch glycolytic). Recent evidence suggests that the principal barrier to O2 diffusion in skeletal muscle resides between the red blood cell and the immediately subjacent sarcolemmal space. Consequently, if the primary design constraint placed on the capillary bed is to facilitate O2 exchange, we hypothesized that capillary surface per fiber surface should be correlated with the mitochondrial volume subserved. Thus, the purpose of this study was to investigate whether one single relationship would be found between the capillary-to-fiber surface ratio and fiber mitochondrial volume in slow- (soleus) and fast-twitch (plantaris) muscle and whether this relationship would be preserved after training. Rats were exercise-trained on a motor-driven treadmill up to 60 min/day, 5 days/week for 4 weeks at an intensity calculated to elicit congruent to 75% VO2max. Following training, soleus (S) and plantaris (P) muscles were removed under deep anesthesia for citrate synthase analysis, and the contralateral limb was perfusion-fixed in situ with glutaraldehyde and analyzed morphometrically under light and electron microscopy. Training significantly (p < 0.05) increased citrate synthase activity and capillary-to-fiber ratio both in S and P muscles. For all muscles combined (i.e., S and P, control and trained), the capillary-to-fiber surface ratio significantly correlated with mitochondrial volume per unit fiber length (r = 0.64). Our finding of a single relationship between the capillary-to-fiber surface ratio and fiber mitochondrial volume across the muscles is consistent with the notion that the size of the capillary bed in muscles comprised principally of either slow-twitch oxidative or mixed fast-twitch oxidative glycolytic and fast-twitch glycolytic fibers is primarily designed to meet fiber requirements for O2 exchange, and that an important site for O2 diffusion resistance is at the capillary-fiber interface. In addition, capillary-to-fiber surface and fiber mitochondrial volume increased in similar proportions, i.e., the relationship between the two variables was preserved after endurance training.